Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar
In perennial trees, wood development is a carbon-demanding process, pivotal for secondary cell wall (SCW) formation and xylem development. Sugars, functioning both as carbon substrates and signaling molecules, orchestrate cambial proliferation and xylem differentiation. However, few molecular candid...
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2025-05-01
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| author | Jing Lu Qiao Ren Qilin Wang Yaqi Wen Yanhong Wang Ruiqi Liang Dingxin Ran Yifeng Jia Xinyu Zhuo Jiangtao Luo Xianqiang Wang Keming Luo |
| author_facet | Jing Lu Qiao Ren Qilin Wang Yaqi Wen Yanhong Wang Ruiqi Liang Dingxin Ran Yifeng Jia Xinyu Zhuo Jiangtao Luo Xianqiang Wang Keming Luo |
| author_sort | Jing Lu |
| collection | DOAJ |
| description | In perennial trees, wood development is a carbon-demanding process, pivotal for secondary cell wall (SCW) formation and xylem development. Sugars, functioning both as carbon substrates and signaling molecules, orchestrate cambial proliferation and xylem differentiation. However, few molecular candidates involved in the sugar-mediated regulation of wood development have been characterized. Cell wall invertases (CWINs), a subclass of the invertase enzyme family localized in the apoplastic space, catalyze the irreversible hydrolysis of sucrose into glucose and fructose, thereby governing carbon allocation in sink tissues. Here, <i>PtoCWIN4</i> shows preferential expression in the stem of <i>Populus tomentosa</i> and has a high efficiency in sucrose cleavage activity. We demonstrated that the knockout of <i>PtoCWIN4</i> results in stunted growth, aberrant branching patterns, and compromised secondary xylem formation. In contrast, mutant lines displayed enhanced SCW thickness accompanied by elevated cellulose and hemicellulose accumulation. Following this, the knockout of <i>PtoCWIN4</i> led to impaired carbon partitioning from sucrose to hexose metabolites during wood development, corroborating the enzyme’s role in sustaining sucrose hydrolysis. Collectively, these findings establish <i>PtoCWIN4</i> as a master regulator of sucrose-to-hexose conversion, a metabolic gateway critical for balancing structural biomass production and developmental growth during wood formation. |
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| language | English |
| publishDate | 2025-05-01 |
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| series | Plants |
| spelling | doaj-art-d2138a972de84d8ea70a3db6426731142025-08-20T01:49:20ZengMDPI AGPlants2223-77472025-05-01149138810.3390/plants14091388Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in PoplarJing Lu0Qiao Ren1Qilin Wang2Yaqi Wen3Yanhong Wang4Ruiqi Liang5Dingxin Ran6Yifeng Jia7Xinyu Zhuo8Jiangtao Luo9Xianqiang Wang10Keming Luo11Chongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaChongqing Key Laboratory of Innovative and Utilization of Forest Germplasm Resources, Integrative Science Center of Germplasm Creation in Western China (Chongqing) Science City, School of Life Sciences, Southwest University, Chongqing 400715, ChinaIn perennial trees, wood development is a carbon-demanding process, pivotal for secondary cell wall (SCW) formation and xylem development. Sugars, functioning both as carbon substrates and signaling molecules, orchestrate cambial proliferation and xylem differentiation. However, few molecular candidates involved in the sugar-mediated regulation of wood development have been characterized. Cell wall invertases (CWINs), a subclass of the invertase enzyme family localized in the apoplastic space, catalyze the irreversible hydrolysis of sucrose into glucose and fructose, thereby governing carbon allocation in sink tissues. Here, <i>PtoCWIN4</i> shows preferential expression in the stem of <i>Populus tomentosa</i> and has a high efficiency in sucrose cleavage activity. We demonstrated that the knockout of <i>PtoCWIN4</i> results in stunted growth, aberrant branching patterns, and compromised secondary xylem formation. In contrast, mutant lines displayed enhanced SCW thickness accompanied by elevated cellulose and hemicellulose accumulation. Following this, the knockout of <i>PtoCWIN4</i> led to impaired carbon partitioning from sucrose to hexose metabolites during wood development, corroborating the enzyme’s role in sustaining sucrose hydrolysis. Collectively, these findings establish <i>PtoCWIN4</i> as a master regulator of sucrose-to-hexose conversion, a metabolic gateway critical for balancing structural biomass production and developmental growth during wood formation.https://www.mdpi.com/2223-7747/14/9/1388poplarxylem developmentSCWsugar metabolismsugar signaling |
| spellingShingle | Jing Lu Qiao Ren Qilin Wang Yaqi Wen Yanhong Wang Ruiqi Liang Dingxin Ran Yifeng Jia Xinyu Zhuo Jiangtao Luo Xianqiang Wang Keming Luo Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar Plants poplar xylem development SCW sugar metabolism sugar signaling |
| title | Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar |
| title_full | Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar |
| title_fullStr | Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar |
| title_full_unstemmed | Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar |
| title_short | Cell Wall Invertase 4 Governs Sucrose–Hexose Homeostasis in the Apoplast to Regulate Wood Development in Poplar |
| title_sort | cell wall invertase 4 governs sucrose hexose homeostasis in the apoplast to regulate wood development in poplar |
| topic | poplar xylem development SCW sugar metabolism sugar signaling |
| url | https://www.mdpi.com/2223-7747/14/9/1388 |
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